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Diaporthe Toxicodendri Sp. Nov., a Causal Fungus of the Canker Disease on Toxicodendron Vernicifluum in Japan Article

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Diaporthe Toxicodendri Sp. Nov., a Causal Fungus of the Canker Disease on Toxicodendron Vernicifluum in Japan Article Mycosphere 8(5): 1157–1167 (2017) www.mycosphere.org ISSN 2077 7019 Article Doi 10.5943/mycosphere/8/5/6 Copyright © Guizhou Academy of Agricultural Sciences Diaporthe toxicodendri sp. nov., a causal fungus of the canker disease on Toxicodendron vernicifluum in Japan Ando Y1, Masuya H1, Aikawa T1, Ichihara Y2 and Tabata M1* 1 Tohoku Research Center, Forestry and Forest Products Research Institute (FFPRI), 92-25 Nabeyashiki, Shimo- kuriyagawa, Morioka Iwate 020-0123, Japan 2 Kansai Research Center, Forestry and Forest Products Research Institute (FFPRI), 68 Nagaikyutaroh, Momoyama, Fushimi, Kyoto, Kyoto 612-0855, Japan Ando Y, Masuya H, Aikawa T, Ichihara Y, Tabata M 2017 – Diaporthe toxicodendri sp. nov., a causal fungus of the canker disease on Toxicodendron vernicifluum in Japan. Mycosphere 8(5), 1157–1168, Doi 10.5943/mycosphere/8/5/6 Abstract We describe for the first time the fungus Diaporthe toxicodendri sp. nov., which causes canker disease on the stems and twigs of Toxicodendron vernicifluum. We conducted a phylogenetic analysis using combined multigene sequence data from the rDNA internal transcribed spacer sequence and partial genes for calmodulin, histone H3, beta-tubulin, and translation elongation factor 1-alpha. The results indicate that D. toxicodendri occupies a monophyletic clade with high support. Although 10 species are phylogenetically closely related to D. toxicodendri, morphological characteristics of size of alpha conidia and lacking of beta and gamma conidia support the distinction of this fungus from those closely related species. No sexual morphic structures have yet been found for the species. The pathogenicity of this species was confirmed by the inoculation test to T. vernicifluum. Key words – Anacardiaceae – canker disease – Diaporthales – Phomopsis – taxonomy Introduction Toxicodendron vernicifluum (Stokes) F.A. Barkley is a deciduous tree belonging to the family Anacardiaceae. The tree has economic and cultural importance as its resin is used to make lacquer (Miyamoto & Kakuda 2008). Recently, outbreaks of a canker disease have occurred at T. vernicifluum plantations in Hokkaido, Aomori, and Iwate Prefectures of northern Japan (Tabata pers. obs., Takemoto et al. 2014). Fungal species of the genus Phomopsis (Sacc.) Bubák have frequently been detected in lesions of the diseased trees, but the causal agent has not previously been identified (Takemoto et al. 2014). The genus name Phomopsis has been used for the asexual morphs of Diaporthe species Nitschke (Diaporthales, Ascomycota). However, due to recent changes of the International Code of Nomenclature for algae, fungi, and plants, the sexual and asexual morphs of a single species must now have the same name (Hawksworth et al. 2011, Wingfield et al. 2012). The name Diaporthe over Phomopsis was proposed for this group due to its prior use (Udayanga et al. 2012, Gomes et al. 2013), and here we follow this suggestion. The genus Diaporthe includes many important pathogens that cause dieback and canker diseases on a wide variety of woody and herbaceous plants (Rehner & Uecker 1994, Udayanga et Submitted 5 September 2017, Accepted 2 November 2017, Published 28 November 2017 Corresponding Author: Masanobu Tabata – e-mail – [email protected] 1157 al. 2011, Gomes et al. 2013). Large numbers of Diaporthe species and their asexual morphs have been described, but their taxonomy is confused. A taxonomic revision of the species and a new delimitation of the genus has been proposed, based on analyses of multi-locus DNA sequence data (e.g. Gomes et al. 2013, Udayanga et al. 2014a, b, Dissanayake et al. 2017). Udayanga et al. (2012) reassessed the species in Diaporthe using multi-locus phylogenetic analysis and proposed the phylogenetic species recognition should be applied to this genus. Gomes et al. (2013) also supported to adopt the phylogenetic species recognition for Diaporthe by multi-locus phylogeny using 243 Diaporthe isolates. Udayanga et al. (2014a, b) promoted this species recognition and resolved species boundaries of taxonomically confused groups, that are D. eres species complex and species on Citrus together with related Diaporthe species. In the most recent phylogenetic study, Dissanayake et al. (2017) revealed taxonomic status of 171 Diaporthe species used available ex-type isolates by multi-locus phylogenetic analysis. Several new species have been described according to this delimitation, especially from Asia (Tan et al. 2013, Gao et al. 2014, 2016, Fan et al. 2015, Udayanga et al. 2015, Du et al. 2016, Tanney et al. 2016). However, many unknown and/or ambiguous species from all over the world are still waiting to be defined and described. Three Diaporthe and 2 Phomopsis species were listed in Japan in 1917 (Shirai & Miyake 1917). Later, Hara (1954) identified 42 more species of Diaporthe and Phomopsis from various woody and herbaceous plants. However, some of these may have been misidentified. Kobayashi (1970) studied the Japanese Diaporthaceae fungi and recognized 19 species in the Diaporthe genus, providing detailed morphological descriptions and illustrations. Thereafter, several additional Diaporthe or Phomopsis species have been reported in fruit trees and agricultural crops in Japan (Kajitani & Kanematsu 2000, Kishi 1998, Katsumoto 2010). Among these, a species of diaportalean fungus associated with Toxicodendron was reported as Diaporthe spiculosa (Westend.) Nitschke (Kobayashi 1970). However, D. spiculosa lacked the asexual morphic state and it was different from the Diaporthe spp. reported as Phomopsis by Takemoto et al. (2014). The aims of the present study are to clarify the taxonomic position of the causal agent of canker disease on Toxicodendron vernicifluum using combined multi-gene sequences as in recent studies (e.g., Gomes et al. 2013, Udayanga et al. 2014b) as well as morphological characteristics and to confirm the pathogenicity of this fungus. Materials & Methods Fungal isolation Eight samples were collected from the stems and twigs of Toxicodendron vernicifluum in the plantations at Hokkaido, Aomori, and Iwate Prefectures in northern Japan. Isolates were obtained from the samples using single conidia or hyphae. For single conidial isolation, spore masses were picked from the samples, suspended in 500 µl distilled water, and streaked onto the 1% malt extract agar (MA) plates. Single hyphae germinated from single conidia were then transferred to 2% MA plates. For single hyphal isolation, tissue fragments were punched out from visible lesions on collected twigs using a 4 mm cork borer. The fragments were immersed in 70% ethanol for 30s and in sodium hypochlorite solution (1% available chlorine) for 3 min, rinsed twice in sterile distilled water, and blotted dry on sterile filter paper for 15 min. Each fragment was placed on the surface of 1% MA plate. The plates were incubated at 15°C in the dark and observed intermittently under a dissecting microscope. Any single hypha growing from a fragment was isolated and transferred to a 2% MA plate and maintained. The pure cultures were used for culture characterization, optimal growth temperature assessment, molecular phylogenetic analysis, and inoculation. Isolates obtained in this study were deposited in the Forestry and Forest Products Research Institute (FFPRI) culture collection at Tsukuba, Japan, or author’s culture collection (AYC). The specimens collected in this study were deposited in the Herbarium of Forest Mycology and Pathology (TFM) of FFPRI. 1158 Table 1 Isolate and GenBank accession numbers used in this study. GenBank accession number b Species Isolate a ITS CAL HIS EF-1α BT D. ampelina CBS 114016 T AF230751 AY745026 – AY745056 JX275452 D. betulicola CFCC 51128 T KX024653 KX024659 KX024661 KX024655 KX024657 D. carpini CBS 114437 KC343044 KC343286 KC343528 KC343770 KC344012 D. detrusa CBS 109770 KC343061 KC343303 KC343545 KC343787 KC344029 D. fibrosa CBS 109751 KC343099 KC343341 KC343583 KC343825 KC344067 D. impulsa CBS 114434 KC343121 KC343363 KC343605 KC343847 KC344089 D. juglandicola CFCC 51134 T KU985101 KX024616 KX024622 KX024628 KX024634 D. padi var. padi CBS 114649 KC343170 KC343412 KC343654 KC343896 KC344138 D. rostrata CFCC 50062 T KP208847 KP208849 KP208851 KP208853 KP208855 D. scobina CBS 251.38 KC343195 KC343437 KC343679 KC343921 KC344163 D. thunbergii MFLUCC 100576 T JQ619893 JX197440 – JX275409 JX275449 D. toxicodendri sp. nov. FFPRI420984 LC275189 LC275197 LC275205 LC275213 LC275221 FFPRI420985 LC275190 LC275198 LC275206 LC275214 LC275222 FFPRI411163 LC275191 LC275199 LC275207 LC275215 LC275223 FFPRI420987 T LC275192 LC275200 LC275208 LC275216 LC275224 FFPRI420990 LC275193 LC275201 LC275209 LC275217 LC275225 FFPRI420991 LC275194 LC275202 LC275210 LC275218 LC275226 FFPRI411164 LC275195 LC275203 LC275211 LC275219 LC275227 FFPRI411165 LC275196 LC275204 LC275212 LC275220 LC275228 D. woolworthii CBS 148.27 KC343245 KC343487 KC343729 KC343971 KC344213 a Ex-type or ex-epitype isolates are marked by T. b Sequences obtained in this study are shown in bold. Morphological observations Samples were dissected and sectioned under a stereomicroscope using flame-sterilized scalpels and tweezers. Fungal structures were mounted in Shear’s fluid (Chupp 1940) on glass slides and observed under a differential interference contrast microscope (Leica DM2500, Leica microsystems Inc.). Fifteen pycnidia and more than 150 conidia were selected randomly and measured to calculate the averages and ranges. In order to determine the optimal temperatures for growth in culture,
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